MODULARITY AND INTEGRATION IN VASCULAR PLANT REPRODUCTIVE STRUCTURES

Many extant plant reproductive structures combine modular construction with functional integration; for example, flowers not only have many parts but also show strong physical and developmental interactions among subsets of those parts. In general, land plants may have evolved reproductive complexity by increasing the number of these modules and the strength of interactions among them, but it is difficult to directly compare reproductive structures through time and across clades because they are highly disparate. Here we use an implementation of graph theory to analyze interactions among plant reproductive parts independently of homology or specific morphologies; we treat parts of a given reproductive structure as nodes and score a set of interaction types among them, including attachment, fusion, envelopment, enclosure, and conforming growth. We then use several metrics (average node degree, total number of interactions, number of node communities) as measures of integration and modularity. We analyzed more than 750 reproductive structures produced by free-sporing plants and seed plants from the Late Silurian through the recent; of these various groups, only those produced by seed plants show an increase in interactions after the Carboniferous. Average degree and number of interactions rise first over the Jurassic with the appearance of derived conifer and “seed fern” groups and then again in the Late Cretaceous with the radiation of derived flowering plants. Seed plants, particularly flowering plants, also show a positive correlation between the number of nodes and communities, suggesting that the evolution of more parts is associated with increased modularity. Modularity itself, however, does not show any obvious trend through time among seed plants until a rise associated with the diversification of flowering plants. These results support the idea that vascular plant reproductive structures as a whole show progressively more functional integration through time, with major shifts occurring in the middle and late Mesozoic. In some clades, this integration may ultimately lead to the formation of new developmental and functional modules, such as the seed or the carpel, which then facilitate further interactions among parts.